Kinetics and mechanics of clot contraction are governed by the molecular and cellular composition of the blood

Blood

Volumn 127, Issue 1, 2016, Pages 149-159

  Tutwiler, Valerie ^a,b   Litvinov, Rustem I ^b   Lozhkin, Andrey P ^c   Peshkova, Alina D ^c   Lebedeva, Tatiana ^d   Ataullakhanov, Fazoil I ^e   Spiller, Kara L ^a   Cines, Douglas B ^d   Weisel, John W ^b  

^a Drexel University   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e HemaCore LLC   (Russian Federation)

Author keywords

A new dynamic quantitative clot contraction assay can reveal novel aspects of formation and evolution of hemostatic clots and thrombi; And various blood components; Clot contraction has 3 phases differentially affected by platelet and fibrin mechanics; RBC compaction

Indexed keywords

ALPHA2B BETA3 INTEGRIN; BLOOD CLOTTING FACTOR 13A; CALCIUM CHLORIDE; CONTRACTILE PROTEIN; FIBRIN; FIBRINOGEN; INTEGRIN; MYOSIN II; MYOSIN IIA; THROMBIN; UNCLASSIFIED DRUG; CALCIUM; CROSS LINKING REAGENT; FIBRINOGEN RECEPTOR;

ARTICLE; BLOOD CLOT; BLOOD COMPONENT; BLOOD FLOWMETRY; BLOOD VESSEL OCCLUSION; CELL COMPOSITION; CONTROLLED STUDY; CROSS LINKING; ERYTHROCYTE; HEMOSTASIS; HUMAN; IN VITRO STUDY; KINETICS; PRIORITY JOURNAL; RATE CONSTANT; THROMBOCYTE; THROMBOCYTE COUNT; THROMBOSIS; VISCOELASTICITY; BLOOD CLOT RETRACTION; BLOOD CLOTTING; CYTOLOGY; FLOW KINETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

BLOOD COAGULATION; BLOOD PLATELETS; CALCIUM; CLOT RETRACTION; CROSS-LINKING REAGENTS; ERYTHROCYTES; FACTOR XIIIA; FIBRIN; HEMOSTASIS; HUMANS; KINETICS; NONMUSCLE MYOSIN TYPE IIA; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; RHEOLOGY; THROMBIN; THROMBOSIS;

EID: 84955459560     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-05-647560     Document Type: Article

References (55)

1. Previtali E, Bucciarelli P, Passamonti SM, Martinelli I. Risk factors for venous and arterial thrombosis. Blood Transfus. 2011;9(2):120-138.
2. ISTH Steering Committee for World Thrombosis Day. Thrombosis: A major contributor to the global disease burden. J Thromb Haemost. 2014;12(10): 1580-1590.
3. Stalker TJ, Welsh JD, Tomaiuolo M, et al. A systems approach to hemostasis: 3. Thrombus consolidation regulates intrathrombus solute transport and local thrombin activity. Blood. 2014; 124(11):1824-1831.
4. Carr ME Jr. Development of platelet contractile force as a research and clinical measure of platelet function. Cell Biochem Biophys. 2003; 38(1):55-78.
5. Lam WA, Chaudhuri O, Crow A, et al. Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat Mater. 2011; 10(1):61-66.
6. Muthard RW, Diamond SL. Blood clots are rapidly assembled hemodynamic sensors: flow arrest triggers intraluminal thrombus contraction. Arterioscler Thromb Vasc Biol. 2012;32(12): 2938-2945.
7. Ĺeon C, Eckly A, Hechler B, et al. Megakaryocyterestricted MYH9 inactivation dramatically affects hemostasis while preserving platelet aggregation and secretion. Blood. 2007;110(9):3183-3191.
8. Seitz R, Duckert F, Lopaciuk S, Muszbek L, Rodeghiero F, Seligsohn U; Study Group. ETRO Working Party on Factor XIII questionnaire on congenital factor XIII deficiency in Europe: status and perspectives. Semin Thromb Hemost. 1996; 22(5):415-418.
9. Schorer AE, Singh J, Basara ML. Dysfibrinogenemia: A case with thrombosis (fibrinogen Richfield) and an overview of the clinical and laboratory spectrum. Am J Hematol. 1995;50(3):200-208.
10. Sutton JT, Ivancevich NM, Perrin SR Jr, Vela DC, Holland CK. Clot retraction affects the extent of ultrasound-enhanced thrombolysis in an ex vivo porcine thrombosis model. Ultrasound Med Biol. 2013;39(5):813-824.
11. Ehrlicher A, Hartwig JH. Cell mechanics: contracting to stiffness. Nat Mater. 2011;10(1): 12-13.
12. Carr ME Jr, Martin EJ, Carr SL. Delayed, reduced or inhibited thrombin production reduces platelet contractile force and results in weaker clot formation. Blood Coagul Fibrinolysis. 2002;13(3): 193-197.
13. Jennings LK, Fox JE, Edwards HH, Phillips DR. Changes in the cytoskeletal structure of human platelets following thrombin activation. J Biol Chem. 1981;256(13):6927-6932.
14. Weisel JW, Litvinov RI. Mechanisms of fibrin polymerization and clinical implications. Blood. 2013;121(10):1712-1719.
15. Brown AEX, Litvinov RI, Discher DE, Purohit PK, Weisel JW. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science. 2009;325(5941):741-744.
16. Kim OV, Litvinov RI, Weisel JW, Alber MS. Structural basis for the nonlinear mechanics of fibrin networks under compression. Biomaterials. 2014;35(25):6739-6749.
17. Bennett JS. Platelet-fibrinogen interactions. Ann N Y Acad Sci. 2001;936:340-354 .
18. Phillips DR, Charo IF, Scarborough RM. GPIIb- IIIa: The responsive integrin. Cell. 1991;65(3): 359-362.
19. Kasahara K, Kaneda M, Miki T, et al. Clot retraction is mediated by factor XIII-dependent fibrin-aIIbb3-myosin axis in platelet sphingomyelin-rich membrane rafts. Blood. 2013;122(19):3340-3348.
20. Kasahara K, Souri M, Miki T, Yamamoto N, Ichinose A. Impaired clot retraction in factor XIII A subunit-deficient mice. Blood. 2010;115(6): 1277-1279.
21. Aleman MM, Byrnes JR, Wang JG, et al. Factor XIII activity mediates red blood cell retention in venous thrombi. J Clin Invest. 2014;124(8): 3590-3600.
22. Byrnes JR, Duval C, Wang Y, et al. Factor XIIIadependent retention of red blood cells in clots is mediated by fibrin a-chain crosslinking. Blood. 2015;126(16):1940-1948.
23. Mackman N. Triggers, targets and treatments for thrombosis. Nature. 2008;451(7181):914-918.
24. Tran R, Myers DR, Ciciliano J, et al. Biomechanics of haemostasis and thrombosis in health and disease: from the macro- To molecular scale. J Cell Mol Med. 2013;17(5):579-596.
25. Stein PD, Beemath A, Meyers FA, Skaf E, Olson RE. Deep venous thrombosis and pulmonary embolism in hospitalized patients with sickle cell disease. Am J Med. 2006;119(10): 897e7-897e11.
26. Cines DB, Lebedeva T, Nagaswami C, et al. Clot contraction: compression of erythrocytes into tightly packed polyhedra and redistribution of platelets and fibrin. Blood. 2014;123(10): 1596-1603.
27. Zabczyk M, Sadowski M, Zalewski J, Undas A. Polyhedrocytes in intracoronary thrombi from patients with ST-elevation myocardial infarction. Int J Cardiol. 2015;179:186-187.
28. Carr ME Jr, Carr SL, Greilich PE. Heparin ablates force development during platelet mediated clot retraction. Thromb Haemost. 1996;75(4):674-678.
29. Suzuki-Inoue K, Hughes CE, Inoue O, et al. Involvement of Src kinases and PLCg2 in clot retraction. Thromb Res. 2007;120(2):251-258.
30. Straight AF, Cheung A, Limouze J, et al. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science. 2003;299(5613):1743-1747.
31. Kovacs M, Toth J, Hetenyi C, Malńasi-Csizmadia A, Sellers JR. Mechanism of blebbistatin inhibition of myosin II. J Biol Chem. 2004;279(34): 35557-35563.
32. Cohen I, Burk DL, White JG. The effect of peptides and monoclonal antibodies that bind to platelet glycoprotein IIb-IIIa complex on the development of clot tension. Blood. 1989;73(7): 1880-1887.
33. Rooney MM, Parise LV, Lord ST. Dissecting clot retraction and platelet aggregation. Clot retraction does not require an intact fibrinogen g chain C terminus. J Biol Chem. 1996;271(15):8553-8555.
34. Carr ME Jr, Carr SL, Hantgan RR, Braaten J. Glycoprotein IIb/IIIa blockade inhibits plateletmediated force development and reduces gel elastic modulus. Thromb Haemost. 1995;73(3): 499-505.
35. Still BM. Experiments on plasma clot contraction. Blood. 1952;7(8):808-815.
36. Rand ML, Leung R, Packham MA. Platelet function assays. Transfus Apheresis Sci. 2003; 28(3):307-317.
37. Paniccia R, Priora R, Liotta AA, Abbate R. Platelet function tests: A comparative review. Vasc Health Risk Manag. 2015;11:133-148.
38. Hayward CPM, Rao AK, Cattaneo M. Congenital platelet disorders: overview of their mechanisms, diagnostic evaluation and treatment. Haemophilia. 2006;12(suppl 3):128-136.
39. Jirouskova M, Dyr JE, Suttnar J, Holada K, Trnkova B. Platelet adhesion to fibrinogen, fibrin monomer, and fibrin protofibrils in flowing blood - The effect of fibrinogen immobilization and fibrin formation. Thromb Haemost. 1997;78(3): 1125-1131.
40. Cho J, Degen JL, Coller BS, Mosher DF. Fibrin but not adsorbed fibrinogen supports fibronectin assembly by spread platelets. Effects of the interaction of alphaIIb beta3 with the C terminus of the fibrinogen gamma-chain. J Biol Chem. 2005; 280(42):35490-35498.
41. Brzoska T, Suzuki Y, Mogami H, Sano H, Urano T. Binding of thrombin-activated platelets to a fibrin scaffold through a(IIb)b3 evokes phosphatidylserine exposure on their cell surface. PLoS One. 2013;8(2):e55466.
42. Mammadova-Bach E, Ollivier V, Loyau S, et al. Platelet glycoprotein VI binds to polymerized fibrin and promotes thrombin generation. Blood. 2015; 126(5):683-691.
43. Ono A, Westein E, Hsiao S, et al. Identification of a fibrin-independent platelet contractile mechanism regulating primary hemostasis and thrombus growth. Blood. 2008;112(1):90-99.
44. Whelihan MF, Mann KG. The role of the red cell membrane in thrombin generation. Thromb Res. 2013;131(5):377-382.
45. Villa CH, Muzykantov VR, Cines DB. The emerging role for red blood cells in haemostasis: opportunity for intervention. ISBT Sci Ser. In press.
46. Kroll MH, Michaelis LC, Verstovsek S. Mechanisms of thrombogenesis in polycythemia vera. Blood Rev. 2015;29(4):215-221.
47. Ilesanmi OO. Pathological basis of symptoms and crises in sickle cell disorder: implications for counseling and psychotherapy. Hematol Rep. 2010;2(1):e2.
48. Maciaszek JL, Andemariam B, Lykotrafitis G. Microelasticity of red blood cells in sickle cell disease. J Strain Anal Eng Des. 2011;46(5): 368-379.
49. Quadros AS, Cambruzzi E, Sebben J, et al. Red versus white thrombi in patients with ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention: clinical and angiographic outcomes. Am Heart J. 2012;164(4): 553-560.
50. Egot M, Kauskot A, Lasne D, Gaussem P, Bachelot-Loza C. Biphasic myosin II light chain activation during clot retraction. Thromb Haemost. 2013;110(6):1215-1222.
51. Litvinov RI, Gorkun OV, Owen SF, Shuman H, Weisel JW. Polymerization of fibrin: specificity, strength, and stability of knob-hole interactions studied at the single-molecule level. Blood. 2005; 106(9):2944-2951.
52. Carvalho FA, Connell S, Miltenberger-Miltenyi G, et al. Atomic force microscopy-based molecular recognition of a fibrinogen receptor on human erythrocytes. ACS Nano. 2010;4(8):4609-4620.
53. Podolnikova NP, Gorkun OV, Loreth RM, Yee VC, Lord ST, Ugarova TP. A cluster of basic amino acid residues in the gamma370-381 sequence of fibrinogen comprises a binding site for platelet integrin alpha(IIb)beta3 (glycoprotein IIb/IIIa). Biochemistry. 2005;44(51):16920-16930.
54. Qiu Y, Brown AC, Myers DR, et al. Platelet mechanosensing of substrate stiffness during clot formation mediates adhesion, spreading, and activation. Proc Natl Acad Sci USA. 2014; 111(40):14430-14435.
55. Biggs R, Macfarlane RG. Human Blood Coagulation and Its Disorders. Oxford: Blackwell; 1953.